Design of a Neuronal Array

Retinal ganglion cells of a given type overlap their dendritic fields such that every point in space is covered by three to four cells. We investigated what function is served by such extensive overlap. Recording from pairs of ON or OFF brisk-transient ganglion cells at photopic intensities, we confirmed that this overlap causes the Gaussian receptive field centers to be spaced at ∼2 SDs (σ). This, together with response nonlinearities and variability, was just sufficient to provide an ideal observer with uniform contrast sensitivity across the retina for both threshold and suprathreshold stimuli. We hypothesized that overlap might maximize the information represented from natural images, thereby optimizing retinal performance for many tasks. Indeed, tested with natural images (which contain statistical correlations), a model ganglion cell array maximized information represented in its population responses with ∼2σ spacing, i.e., the overlap observed in the retina. Yet, tested with white noise (which lacks statistical correlations), an array maximized its information by minimizing overlap. In both cases, optimal overlap balanced greater signal-to-noise ratio (from larger receptive fields) against greater redundancy (because of larger receptive field overlap). Thus, dendritic overlap improves vision by taking optimal advantage of the statistical correlations of natural scenes.

[1]  David J. Braverman,et al.  Learning Filters for Optimum Pattern Recognition , 1962, IRE Trans. Inf. Theory.

[2]  W. A. Hagins,et al.  Kinetics of the photocurrent of retinal rods. , 1972, Biophysical journal.

[3]  David G. Stork,et al.  Pattern Classification , 1973 .

[4]  H. Wässle,et al.  The distribution of the alpha type of ganglion cells in the cat's retina , 1975, The Journal of comparative neurology.

[5]  Allan W. Snyder,et al.  Information capacity of eyes , 1977, Vision Research.

[6]  H. Wässle,et al.  Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. , 1979, The Journal of physiology.

[7]  B. Boycott,et al.  Morphology and topography of on- and off-alpha cells in the cat retina , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[8]  B. Boycott,et al.  Dendritic territories of cat retinal ganglion cells , 1981, Nature.

[9]  R. Linden,et al.  Evidence for dendritic competition in the developing retina , 1982, Nature.

[10]  Edward H. Adelson,et al.  Saturation and adaptation in the rod system , 1982, Vision Research.

[11]  S. Laughlin,et al.  Predictive coding: a fresh view of inhibition in the retina , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[12]  P. Lennie,et al.  The influence of temporal frequency and adaptation level on receptive field organization of retinal ganglion cells in cat , 1982, The Journal of physiology.

[13]  W A Richards,et al.  Lightness scale from image intensity distributions. , 1981, Applied optics.

[14]  S. Laughlin,et al.  Matching Coding to Scenes to Enhance Efficiency , 1983 .

[15]  D. Mastronarde Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. , 1983, Journal of neurophysiology.

[16]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[17]  G. J. Burton,et al.  Color and spatial structure in natural scenes. , 1987, Applied optics.

[18]  D J Field,et al.  Relations between the statistics of natural images and the response properties of cortical cells. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[19]  K. Yau,et al.  Light adaptation in cat retinal rods. , 1989, Science.

[20]  D. Dacey,et al.  Monoamine‐accumulating ganglion cell type of the cat's retina , 1989, The Journal of comparative neurology.

[21]  W. Geisler Sequential ideal-observer analysis of visual discriminations. , 1989, Psychological review.

[22]  Joseph J. Atick,et al.  Towards a Theory of Early Visual Processing , 1990, Neural Computation.

[23]  P. Sterling,et al.  "Collective coding" of correlated cone signals in the retinal ganglion cell. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[24]  K. Yau,et al.  Light Adaptation in Retinal Rods of the Rabbit and Two Other Nonprimate Mammals Nakatani Et Al. Light Adaptation M Rabbit and Other Mammalian Rods Experiments on Cattle and Rat , 1991 .

[25]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[26]  D. I. Vaney,et al.  Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin , 1991, Neuroscience Letters.

[27]  S S Saunders,et al.  Discrimination performance of single neurons: rate and temporal-pattern information. , 1991, Journal of neurophysiology.

[28]  B. Boycott,et al.  Functional architecture of the mammalian retina. , 1991, Physiological reviews.

[29]  L. Peichl,et al.  Alpha ganglion cells in mammalian retinae: Common properties, species differences, and some comments on other ganglion cells , 1991, Visual Neuroscience.

[30]  J. V. van Hateren,et al.  Real and optimal neural images in early vision , 1992, Nature.

[31]  Peter Sterling,et al.  Parallel Circuits from Cones to the On‐Beta Ganglion Cell , 1992, The European journal of neuroscience.

[32]  Zhaoping Li,et al.  Understanding Retinal Color Coding from First Principles , 1992, Neural Computation.

[33]  D. Dacey,et al.  A coupled network for parasol but not midget ganglion cells in the primate retina , 1992, Visual Neuroscience.

[34]  J. H. van Hateren,et al.  Real and optimal neural images in early vision , 1992, Nature.

[35]  P Sterling,et al.  Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[36]  J. V. van Hateren,et al.  Spatiotemporal contrast sensitivity of early vision , 1993, Vision Research.

[37]  DI Vaney,et al.  Territorial organization of direction-selective ganglion cells in rabbit retina , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  S. Laughlin Matching coding, circuits, cells, and molecules to signals: General principles of retinal design in the fly's eye , 1994, Progress in Retinal and Eye Research.

[39]  D. Dacey Physiology, morphology and spatial densities of identified ganglion cell types in primate retina. , 1994, Ciba Foundation symposium.

[40]  D. Baylor,et al.  Concerted Signaling by Retinal Ganglion Cells , 1995, Science.

[41]  I. Ohzawa,et al.  Receptive-field dynamics in the central visual pathways , 1995, Trends in Neurosciences.

[42]  G Buchsbaum,et al.  How retinal microcircuits scale for ganglion cells of different size , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  William B. Levy,et al.  Energy Efficient Neural Codes , 1996, Neural Computation.

[44]  M. Meister Multineuronal codes in retinal signaling. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Distribution and coverage of beta cells in the cat retina. , 1996, The Journal of comparative neurology.

[46]  D. Baylor,et al.  Mosaic arrangement of ganglion cell receptive fields in rabbit retina. , 1997, Journal of neurophysiology.

[47]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[48]  J. V. van Hateren,et al.  Independent component filters of natural images compared with simple cells in primary visual cortex , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  Michael J. Berry,et al.  The Neural Code of the Retina , 1999, Neuron.

[50]  S. DeVries Correlated firing in rabbit retinal ganglion cells. , 1999, Journal of neurophysiology.

[51]  J. B. Demb,et al.  Functional Circuitry of the Retinal Ganglion Cell's Nonlinear Receptive Field , 1999, The Journal of Neuroscience.

[52]  E J Chichilnisky,et al.  A simple white noise analysis of neuronal light responses , 2001, Network.

[53]  Shigeo Abe DrEng Pattern Classification , 2001, Springer London.

[54]  Michael J. Berry,et al.  Metabolically Efficient Information Processing , 2001, Neural Computation.

[55]  R. Wong,et al.  Cell-type specific dendritic contacts between retinal ganglion cells during development. , 2001, Journal of neurobiology.

[56]  S. Laughlin,et al.  An Energy Budget for Signaling in the Grey Matter of the Brain , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[57]  E. Chichilnisky,et al.  Functional Asymmetries in ON and OFF Ganglion Cells of Primate Retina , 2002, The Journal of Neuroscience.

[58]  Roland J. Baddeley,et al.  Synaptic energy efficiency in retinal processing , 2003, Vision Research.

[59]  Peter Sterling,et al.  Contrast threshold of a brisk-transient ganglion cell in vitro. , 2003, Journal of neurophysiology.

[60]  J. B. Demb,et al.  Different Circuits for ON and OFF Retinal Ganglion Cells Cause Different Contrast Sensitivities , 2003, The Journal of Neuroscience.

[61]  M. Schnitzer,et al.  Multineuronal Firing Patterns in the Signal from Eye to Brain , 2003, Neuron.

[62]  N. Grzywacz,et al.  Power spectra and distribution of contrasts of natural images from different habitats , 2003, Vision Research.

[63]  E. Chichilnisky,et al.  Temporal Resolution of Ensemble Visual Motion Signals in Primate Retina , 2003, The Journal of Neuroscience.

[64]  Gonzalo G de Polavieja Reliable biological communication with realistic constraints. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[65]  Bin Lin,et al.  Retinal Ganglion Cell Type, Size, and Spacing Can Be Specified Independent of Homotypic Dendritic Contacts , 2004, Neuron.

[66]  Robert G. Smith,et al.  Spike Generator Limits Efficiency of Information Transfer in a Retinal Ganglion Cell , 2004, The Journal of Neuroscience.

[67]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[68]  P. Sterling,et al.  Efficiency of Information Transmission by Retinal Ganglion Cells , 2004, Current Biology.

[69]  E. Chichilnisky,et al.  Detection Sensitivity and Temporal Resolution of Visual Signals near Absolute Threshold in the Salamander Retina , 2022 .

[70]  Robert A. Frazor,et al.  Independence of luminance and contrast in natural scenes and in the early visual system , 2005, Nature Neuroscience.

[71]  William B. Kristan,et al.  Quantifying Stimulus Discriminability: A Comparison of Information Theory and Ideal Observer Analysis , 2005, Neural Computation.

[72]  Peter Sterling,et al.  Encoding Light Intensity by the Cone Photoreceptor Synapse , 2005, Neuron.

[73]  E. Chichilnisky,et al.  Fidelity of the ensemble code for visual motion in primate retina. , 2005, Journal of neurophysiology.

[74]  P. Sterling,et al.  Chromatic Properties of Horizontal and Ganglion Cell Responses Follow a Dual Gradient in Cone Opsin Expression , 2006, The Journal of Neuroscience.

[75]  P. Sterling,et al.  How Much the Eye Tells the Brain , 2006, Current Biology.

[76]  Jonathon Shlens,et al.  The Structure of Multi-Neuron Firing Patterns in Primate Retina , 2006, The Journal of Neuroscience.

[77]  Jay Z. Parrish,et al.  The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance , 2006, Nature.

[78]  Wei Li,et al.  Parallel Processing in Two Transmitter Microenvironments at the Cone Photoreceptor Synapse , 2006, Neuron.

[79]  G D Field,et al.  Information processing in the primate retina: circuitry and coding. , 2007, Annual review of neuroscience.

[80]  David J. Calkins,et al.  Microcircuitry for Two Types of Achromatic Ganglion Cell in Primate Fovea , 2007, The Journal of Neuroscience.

[81]  Mokshay M. Madiman,et al.  Generalized Entropy Power Inequalities and Monotonicity Properties of Information , 2006, IEEE Transactions on Information Theory.